Effects of voltinism, interspecific competition and parasitism on the population dynamics of the hemlock scales, Fiorinia externa and Tsugaspidiotus tsugae (Homoptera: Diaspididae)

Abstract.

• 1 Life tables were constructed for solitary and coexisting populations of univoltine Fiorinia externa Ferris and bivoltine Tsugaspidiotus tsugae (Marlatt) (Homoptera: Diaspididae), two exotic scale pests of eastern hemlock, Tsuga canadensis Carriere, in the northeastern United States.
• 2 Solitary and coexisting populations of F. externa had similar survivorship and population growth rates resulting in an annual increase in density of 7–16%. Survivorship of solitary and coexisting populations of T. tsugae also was similar, but growth rates differed substantially. While solitary populations increased their density by 68% annually, populations coexisting with F. extema were reduced 74% each year.
• 3 The annual reduction in T. tsugae density where it coexists with F. externa was due in part to interspecific competition which resulted in higher mortality to nymphs from dispersal and starvation and in lower fecundity of adult females relative to solitary populations. A host shift by the parasitoid, Aspidiotiphagus citrinus (Crawford) (Hymenoptera: Aphenlinidae) from F. externa to T. tsugae in autumn also accounted for 71% of the annual decrease in T. tsugae numbers. Therefore, F. externa adversely affects the growth of T. tsugae populations not only because of its superior competitive ability but also because adult para-sitoids which emerge from it subsequently attack nymphs of T. tsugae in autumn.
• 4 Parasitism and starvation of nymphs resulting from competition were the key mortality factors in the population dynamics of these exotic hemlock scales.

     

Fitness and physiology of Adelges tsugae (Hemiptera: Adelgidae) in relation to the health of the eastern hemlock

The hemlock woolly adelgid, Adelges tsugae Annand is an invasive insect that frequently causes hemlock (Tsuga spp.) mortality in the eastern United States. Studies have shown that once healthy hemlocks become infested by the adelgid, nutrients are depleted from the tree, leading to both tree decline and a reduction of the adelgid population. Since A. tsugae is dependent on hemlock for nutrients, feeding on trees in poor health may affect the ability of the insect to obtain necessary nutrients and may consequently affect their physiological and population health. Trees were categorized as lightly or moderately impacted by A. tsugae based on quantitative and qualitative tree health measurements. Population health of A. tsugae on each tree was determined by measuring insect density and peak mean fecundity; A. tsugae physiological health was determined by measuring insect biomass, total carbon, carbohydrate, total nitrogen, and amino nitrogen levels. Adelges tsugae from moderately impacted trees exhibited significantly greater fecundity than from lightly impacted trees. However, A. tsugae from lightly impacted hemlocks contained significantly greater levels of carbohydrates, total nitrogen, and amino nitrogen. While the results of the physiological analysis generally support our hypothesis that A. tsugae on lightly impacted trees are healthier than those on moderately impacted trees, this was not reflected in the population health measurements. Adelges tsugae egg health in response to tree health should be verified. This study provides the first examination of A. tsugae physiological health in relation to standard A. tsugae population health measures on hemlocks of different health levels.     

Asymmetric priority effects influence the success of invasive forest insects

1. Settlement timing is often an important factor in interspecific herbivore interactions, as early‐arriving species may encounter higher resource availability and/or avoid induced defences. Despite the general importance of priority effects to the outcome of herbivore interactions, there has been little exploration of such interactions on woody host plants where their impact can only be measured over multiple years. 2. In the eastern U.S.A., two invasive species, the hemlock woolly adelgid Adelges tsugae and the elongate hemlock scale Fiorinia externa, share a native host, eastern hemlock Tsuga canadensis. Their interaction and its consequences were investigated for plant growth – hemlock saplings that had been inoculated with either A. tsugae or F. externa, starting in spring 2007, were cross‐infested with the other insect in spring 2009. A set of uninfested trees was simultaneously infested with A. tsugae, F. externa, both, or neither insect (= control), and insect density and plant growth was assessed in all treatments. 3. Adelges tsugae settlement rates did not differ if it settled alone or simultaneously with F. externa, but were ～45% lower on trees previously infested with F. externa. There was no difference in F. externa settlement rates, and plant growth did not differ substantively between any of the herbivore treatments. 4. At a temporal scale (i.e. multiple growing seasons) appropriate to interactions between woody plants and their herbivores, this work demonstrates that plant‐mediated priority effects can substantially affect herbivore settlement and thus the outcome of interspecific competition.     

Range expansion and population dynamics of co-occurring invasive herbivores

Although a range of studies have suggested that competition plays a critical role in determining herbivore assemblages, there has been little work addressing the nature of interactions between competing invasive herbivores. We report the results of research on the hemlock woolly adelgid Adelges tsugae (‘HWA’) and elongate hemlock scale Fiorinia externa (‘EHS’), invasive herbivores that both feed on eastern hemlock (Tsuga canadensis). HWA has been linked to hemlock mortality throughout the East Coast of the US; the loss of hemlock threatens to permanently alter surrounding ecosystems. We assessed the spread and impact of both species by resurveying 142 hemlock stands across a 7,500 km² latitudinal transect, running from coastal CT to northern MA, for HWA and EHS density as well as hemlock mortality. These stands had been previously surveyed in either 1997–1998 (CT) or 2002–2004 (MA). While the number of HWA-infested stands has increased, per-stand HWA density has substantially decreased. In contrast, EHS distribution and density has increased dramatically since 1997–1998. Hemlock mortality was much more strongly related to HWA density than to EHS density, and many stands remain relatively healthy despite an overall increase in hemlock mortality. There was a positive correlation between HWA and EHS densities in stands with low mean HWA densities, suggesting the potential for host-plant-mediated facilitation of EHS by HWA. Our findings underline the importance of research explicitly addressing interactions between competing invasive species, and of determining the potential consequences of these interactions for the invaded ecosystem.     

Competitor avoidance drives within‐host feeding site selection in a passively dispersed herbivore

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Simulating the dispersal of hemlock woolly adelgid in the temperate forest understory

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Fungi associated with a natural epizootic in Fiorinia externa Ferris (Hemiptera: Diaspididae) populations

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Facilitation between invasive herbivores: hemlock woolly adelgid increases gypsy moth preference for and performance on eastern hemlock

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Effects of population density on male and female reproductive success in the wind-pollinated, wind-dispersed tree species Betula maximowicziana

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Tree responses to an invasive sap-feeding insect

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The influence of seed dispersal mechanisms on the genetic structure of tropical tree populations

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Factors affecting settlement rate of the hemlock woolly adelgid,Adelges tsugae,on eastern hemlock,Tsuga canadensis

1 We assessed the importance of several factors potentially affecting the settlement rate of the invasive hemlock woolly adelgid Adelges tsugae (Hemiptera: Adelgidae) on uninfested foliage of the eastern hemlock, Tsuga canadensis. We conducted our experiments in Massachusetts (U.S.A.) with overwintering sistens adelgids, and applied standard densities of infested foliage to uninfested branches in a planned multiple‐comparison design. 2 Settlement rates of progrediens crawlers produced by the overwintering sistens were highest when adelgid‐infested foliage was loosely attached to uninfested foliage and both branches were then enclosed in a mesh sleeve. 3 Early‐emerging crawlers settled at a higher rate than did late‐emerging crawlers. 4 Increasing the density of infested branches did not affect settlement rates. 5 We also tested whether less severe winter conditions improved settlement, and found that overwintering infested foliage in a refrigerator decreased settlement rate relative to foliage overwintered outdoors. 6 Our results suggest a protocol for adelgid inoculations that could substantially increase the success rate of experimental manipulations and encourage additional research on the population dynamics of this pest.     

Low plant density enhances gene dispersal in the Amazonian understory herb Heliconia acuminata

In theory, conservation genetics predicts that forest fragmentation will reduce gene dispersal, but in practice, genetic and ecological processes are also dependent on other population characteristics. We used Bayesian genetic analyses to characterize parentage and propagule dispersal in Heliconia acuminata L. C. Richard (Heliconiaceae), a common Amazonian understory plant that is pollinated and dispersed by birds. We studied these processes in two continuous forest sites and three 1‐ha fragments in Brazil's Biological Dynamics of Forest Fragments Project. These sites showed variation in the density of H. acuminata. Ten microsatellite markers were used to genotype flowering adults and seedling recruits and to quantify realized pollen and seed dispersal distances, immigration of propagules from outside populations, and reproductive dominance among parents. We tested whether gene dispersal is more dependent on fragmentation or density of reproductive plants. Low plant densities were associated with elevated immigration rates and greater propagule dispersal distances. Reproductive dominance among inside‐plot parents was higher for low‐density than for high‐density populations. Elevated local flower and fruit availability is probably leading to spatially more proximal bird foraging and propagule dispersal in areas with high density of reproductive plants. Nevertheless, genetic diversity, inbreeding coefficients and fine‐scale spatial genetic structure were similar across populations, despite differences in gene dispersal. This result may indicate that the opposing processes of longer dispersal events in low‐density populations vs. higher diversity of contributing parents in high‐density populations balance the resulting genetic outcomes and prevent genetic erosion in small populations and fragments.     

Interactions of colonisation density and leaf environments on survival of Trioza eugeniae nymphs

1. Female eugenia psyllids Trioza eugeniae oviposit on the margins of expanding young Syzygium paniculatum leaves. The developing nymphs, feeding within pit‐shaped galls on the leaves, cause the leaves to become curled and deformed. The degree of leaf curling was correlated positively with densities of T. eugeniae nymphs. 2. High relative humidity increased persistence of nymphs on leaves at low insect densities, but persistence did not differ between high or low relative humidity conditions when nymphal densities were high and leaves were greatly curled. 3. Direct insolation increased nymphal mortality. Nymphs on the abaxial leaf surface in the direct sun had lower mortality than similarly exposed nymphs on the adaxial leaf surface. 4. Field populations showed high preference for abaxial leaf surfaces and a stronger preference for shaded adaxial surfaces than for exposed adaxial surfaces. 5. Adverse environmental conditions of direct insolation and low relative humidity may be mitigated by leaf curl associated with moderate populations, however competition at high nymphal density supersedes any potential benefit arising from leaf curling and has a negative effect on nymphal survival.     

Forest decline after a 15-year “perfect storm” of invasion by hemlock woolly adelgid,drought, and hurricanes

Invasions by introduced pests can interact with other disturbances to alter forests and their functions, particularly when a dominant tree species declines. To identify changes after invasion by the insect hemlock woolly adelgid (Adelges tsugae; HWA), coinciding with severe droughts and hurricanes, this study compared tree species composition of eastern hemlock (Tsuga canadensis) forests on 11 plots before (2001) and 15 years after (2016) invasion in the southern Appalachian Mountains, USA. Losses of hemlock trees after HWA invasion were among the highest reported, with a 90% decline in density, 86% decline in basal area, and 100% mortality for individuals ≥ 60 cm in diameter. In contrast to predictions of theoretical models, deciduous tree density declined after HWA invasion, while basal area changed little, at least during the initial 15 years after invasion. Overall, forest density declined by 58%, basal area by 25%, and tree species richness by 8%. Factors additional to HWA likely exacerbating forest decline included: droughts before (1999–2001) and after HWA invasion (2006–2008); tree uprooting from hurricane-stimulated winds in 2004; pest-related declines of deciduous tree species otherwise likely benefitting from hemlock’s demise; death of deciduous trees when large hemlocks fell; and competition from aggressive understory plants including doghobble (Leucothoe fontanesiana), rosebay rhododendron (Rhododendron maximum), and Rubus spp. Models of forest change and ecosystem function should not assume that deciduous trees always increase during the first decades after HWA invasion.     

Densities of Two Frugivorous Primates with Respect to Forest and Fragment Tree Species Composition and Fruit Availability

Conservation of wildlife populations requires extensive knowledge of their habitat requirements, efficient methods to evaluate habitat quality, and an understanding of the value of fragments and edges. Kibale National Park, Uganda has areas that differ in the densities of 2 species of frugivorous monkeys—Cercopithecus mitis and Lophocebus albigena—including one on an edge and forest fragments outside the park that lack both species. We compared the basal area densities of important food trees with primate densities. The density of Cercopithecus mitis correlates most strongly with the basal area density of all types of food trees combined. The density of Lophocebus albigena does not correlate with the basal area densities of any category of food trees or with fruit availability. An index of their density—number of groups seen per km walked—correlates to fruit availability but with marginal significance. Lack of a relationship between the basal area densities of food trees and density of Lophocebus albigena may be the result of a mismatch in scale between the forest area measured and their large home ranges. We compared the unused area of forest to the other areas of the forest and the fragments and found it had higher basal area densities in all food tree categories for both species than the fragments and lower basal area densities of most categories than the other parts of the forest, indicating that the fragments are poor quality and would probably be unused even if dispersal were likely.     

Foliar terpenoids in Tsuga species and the fecundity of scale insects

Summary The relationship between the reproductive success of two Japanese scale insects, Fiorinia externa Ferris and Nuculaspis tsugae (Marlatt) (Homoptera: Diaspididae) and the concentrations of 15 terpenoids in needles of Tsuga sieboldii, the Japanese host, and T. canadensis, the North American host, was investigated during 1981 and 1982 in a field plot of 8-year-old trees in New Haven, CT, USA. Both scales produced significantly more eggs per female on T. sieboldii than on T. canadensis. Stepwise multiple regression analyses indicated that the variation in fecundity within both scales was strongly associated with variation in the terpenoid profile between tree species.General patterns of phytochemical variation between the two Tsuga species based on differences in the concentration of terpenoids having similar chemical structures were revealed by the multivariate statistical technique, principal components analysis. The volatile leaf oil profile of T. sieboldii was relatively richer in terpene alcohols, while that of T. canadensis was relatively richer in terpene hydrocarbons and terpene acetates. The individual terpenoids were then assigned to one of five groups based on chemical structure and regression analyses were repeated; fecundity of both scales increased with increasing concentration of terpenoid alcohols. Fecundity of F. externa was negatively associated with the relative concentration of acyclic terpenes but the opposite was true for N. tsugae. Analysis of foliar terpenoids may provide a basis for predicting the relative susceptibility of Tsuga species to attack by F. externa and N. tsugae.     

Seed Dispersal of a High Quality Fruit by Specialized Frugivores: High Quality Dispersal?1

Dispersal quality, as estimated by the cumulative effects of dispersal, germination, seed predation, and seedling survival, was examined for Beilschmiedia pendula (Lauraceae) in Monteverde, Costa Rica. I determined the pattern of dispersal by finding seeds deposited by birds, protected the seeds from seed predators with cages to assess germination and seedling survival, and examined seed predation rates with marked seeds. Seed predation, germination, and seedling survival were compared between seeds naturally dispersed by birds and seeds placed at randomly located sites. Approximately 70 percent of seeds dispersed by birds (N= 244) were deposited <10 m from crown edges of fruiting B. pendula trees, although some seeds were dispersed at least 70 m away. Larger seeds were more likely to be dispersed under or close to the parent trees, and larger seeds produced larger seedlings. Seed size was not correlated directly with seedling survival, but larger seedlings at three months were most likely to survive one year. Seed predation by mammals and insects and seedling mortality due to fungal pathogens were concentrated beneath the crowns of parent trees. Seedlings and saplings were more abundant beneath fruiting B. pendula trees, but individuals farther away were taller on average. Thus, dispersal is beneficial for B. pendula, but such benefits appear most pronounced at a small spatial scale; seeds dispersed >30 m from the crown edges actually had a lower probability of survival than those dispersed 10–20 m. Only 10 percent of B. pendula. seeds received high‐quality dispersal in terms of landing in the zone with the highest per seed probability of seedling survival 10–20 m from parental crowns.